About the Companion Website xvii

1 Order Strepsiptera 1

1.1 Introduction 1

1.2 Are Strepsiptera Parasites or Parasitoids? 10

1.3 Trichotomous Hypothesis of Insect Parasitoids 11

1.4 Metamorphosis 14

References 16

2 History of Strepsiptera 23

References 33

3 Collection 39

3.1 Introduction 39

3.2 Stylopised Leaf- and Planthoppers 39

3.3 Stylopised Eusocial Wasps 40

3.4 Stylopised Grasshoppers/Crickets/Mantids 41

3.5 Stylopised Silverfish 42

References 43

4 Phylogeny 45

4.1 Phylogenetic Position on the Tree of Life 45

4.2 Phylogeny of Strepsiptera 49

4.3 Mitochondrial Genomes 53

References 56

5 Fossil Species 63

5.1 Introduction 63

5.2 Families: Protoxenidae, Phthanoxenidae and Cretostylopidae 67

5.3 Family Mengeidae 69

5.4 Planidia from Cretaceous Amber 71

5.5 Planidium from Eocene Baltic Amber 72

5.6 Males in Eocene Baltic Amber 72

5.7 Males in Compressed Shale 73

5.8 Male in Fushun Amber 76

5.9 Males in Miocene Amber 76

5.10 Male in Madagascar Copal 80

5.11 Fossil Strepsiptera and Their Hosts 80

5.12 Biology of Fossil Strepsiptera 81

References 82

6 First Instar Free- Living Planidium 87

6.1 Introduction 87

6.2 History 89

6.3 Biology and Life History 90

6.4 Birth of Planidia 93

6.5 Locomotion 93

6.6 Entry into Host 94

6.7 Host Defence 97

6.8 Moulting After Host Entry 97

6.9 Dispersal 98

6.9.1 Phoretic Transmission 98

6.9.2 Mass/Direct Release 101

6.10 Planidia Found in Unusual Destinations 101

References 102

7 Endoparasitic Larval Stages 111

7.1 Introduction 111

7.2 Apolysis Without Ecdysis 111

7.3 Life History 115

7.3.1 Endoparasitic Second Instar Larva 115

7.3.2 Endoparasitic Third Instar Larva 115

7.3.3 Endoparasitic Fourth Instar Larva 116

7.4 Internal Development 118

7.5 Emergence and Extrusion Through Host Cuticle 121

7.6 Avirulence 121

7.7 Immune Defence 123

7.7.1 Masquerading as ‘Self’ 123

References 126

8 Pupal Stage 133

8.1 Introduction 133

8.2 Free – Living Puparium of Male and Female Mengenillidae 133

8.3 Partially Endoparasitic Male Puparium of Stylopidia 136

8.4 Pre-formed ‘Line of Weakness’ in Male Puparium of Stylopidia 137

8.5 Development of the Eye in Male Pupa of Stylopidia 140

8.6 Development of the Reproductive System in Male Pupa of Stylopidia 141

8.7 Absence of the Pupal Instar in Female Stylopiformia 141

References 145

9 Adult Male 149

9.1 Introduction 149

9.2 Biology and Life History 152

9.2.1 Head 152

9.2.2 Eyes 153

9.2.3 Thorax 157

9.2.4 Abdomen 161

9.2.5 Reproductive System 163

9.3 Emergence of Free- Living Male from the Puparium 167

9.3.1 Contractions 167

9.3.2 Frontal Sac 167

9.3.3 Mandibles 168

References 169

10 Free- Living Female Mengenillidae and Neotenic Female Stylopidia 177

10.1 Introduction 177

10.2 Free- Living Female Mengenillidae 179

10.3 Endoparasitic, Neotenic Female Stylopidia 180

10.3.1 Reproductive System in Stylopidia 184

10.4 Metamorphic Transformation of the Cephalothorax 186

10.4.1 Developmental Process in Stylopidia 192

10.5 Multiple Cuticles of the Endoparasitic, Neotenic Female Stylopidia 195

10.6 Brood Canal System in Stylopidia 196

10.6.1 Invagination in the Brood Canal of Stylops 198

10.7 Birth of Planidia in Mengenillidae and Stylopidia 199

10.8 Nassonov’s Glands 199

10.8.1 Structure of Nassonov’s Glands 199

10.8.2 Pheromone 202

10.8.3 Structure of the Pheromone 203

References 204

11 Mating 213

11.1 Introduction 213

11.2 Maturation of Male and Female 213

11.3 Female ‘Calling’ Behaviour and Attraction 214

11.4 Adult Male Emergence and Behaviour Before Mating 217

11.5 Behaviour of Male During Mating 218

11.6 Insemination 219

11.6.1 Traumatic Insemination in Mengenillidae 223

11.6.2 Brood Canal Insemination in Stylopidia 223

11.7 Receptor Systems and Signals During Sexual Communication 225

11.7.1 Antennae and Maxillary Palps 225

11.7.2 Tarsi 225

11.7.3 Hairs on Aedeagus 226

11.8 Reproductive Synchrony 226

References 228

12 Basal Extant Families: Family Bahiaxenidae 235

12.1 Introduction and Taxonomy 235

Reference 235

13 Family Mengenillidae 237

13.1 Introduction 237

13.2 Taxonomy 242

13.3 Biology and Life History 245

13.4 Birth and Emergence of Planidia from a Free- Living, Neotenic Female 247

13.4.1 Neotenic Female that Remains in the Puparium 247

13.4.2 Birth and Emergence of Planidia from a Female that Remains in the Puparium 248

13.5 Hosts 249

13.6 Entomophagous Parasites 250

13.7 Nematode Parasites 251

References 252

14 Suborder Stylopidia: Family Corioxenidae 257

14.1 Introduction 257

14.2 Taxonomy 257

14.3 Extrusion of the Cephalotheca and Cephalothorax 260

14.4 Emergence of Male 262

14.5 Unusual Insemination 262

14.6 Emergence of Planidia 263

14.7 Unusual Life Cycle and Super-stylopisation in Blissoxenos 264

14.8 Dispersal of Planidia 267

14.9 Morphological Changes of Stylopised Corioxenidae 267

14.10 Corioxenidae as Biocontrol Agents 268

References 268

15 Infraorder Stylopiformia: Myrmecolacidae 273

15.1 Introduction 273

15.2 Taxonomy 281

15.3 Heterotrophic Heteronomy 285

15.4 Behaviour of Stylopised Ants 288

15.5 Host- Seeking Behaviour of Planidia with Dimorphic Hosts 290

15.6 Cryptic Diversity 291

15.7 Partitioning of Genetic Diversity and Patterns of Host Specificity 292

15.8 Biogeography 299

15.9 Origin of Caenocholax in United States 300

15.10 Multi-parasitism 301

15.11 Myrmecolacidae as Biocontrol Agents 301

References 303

16.1 Family Lychnocolacidae 313

16.1.1 Introduction 313

References 314

16.2 Family Bohartillidae 316

16.2.1 Introduction 316

References 317

17 Family Stylopidae 319

17.1 Introduction 319

17.2 Taxonomy 322

17.3 Prevalence of Stylopisation 324

17.4 Morphological Changes in Stylopised Hosts 324

17.5 Pheromone 327

17.6 Behavioural Changes in Stylopised Hosts 329

17.7 Protandry 330

17.8 Phoretic Transmission 333

17.9 Host- seeking by Planidia 337

17.10 Super-stylopisation 337

17.11 Multi-parasitisim 338

17.12 Cryptic Species and Host Specificity 339

References 341

18 Family Xenidae 351

18.1 Introduction 351

18.2 Taxonomy 354

18.3 Inquilines 359

18.4 Life Cycle of Xenos in Relation to Colony Cycle of Host 360

18.5 Infective Stages of Host 364

18.6 Stylopisation of Polistes in Native and Invasive Ranges 365

18.7 Prevalence 366

18.8 Morphological Changes in Styopised Hosts 369

18.9 Behavioural Changes in Stylopised Hosts 372

18.9.1 Extranidal Aggregations 372

18.9.2 Extended Phenotype 375

18.10 Voltinism 376

18.11 Extension of Life Cycle of Stylopised Host 378

18.12 Virulence 381

18.13 Encapsulation 383

18.14 Effect of Stylopisation on Status Badges 384

18.15 Cuticular Hydrocarbons in Stylopised Hosts 385

18.16 Mechanism of Transfer of Planidia to Nests 385

18.16.1 Phoretic Transmission 386

18.16.2 Mass/Direct Release 390

18.17 Super-stylopisation 391

18.18 Co- Habitation 392

18.19 Phylogeny, Cryptic Species and Host Specificity 392

References 394

19 Family Elenchidae 417

19.1 Introduction and History 417

19.2 Taxonomy 419

19.3 Biology and Life History 421

19.4 Morphological Changes in Stylopised Hosts 423

19.5 Super-stylopisation 424

19.6 Mulit-parasitism 425

19.7 Cryptic Species and Host Specificity 425

19.8 Elenchus as Biocontrol Agents 426

19.9 Wolbachia Endosymbionts 426

References 428

20 Family Halictophagidae 435

20.1 Introduction 435

20.2 Taxonomy 436

20.3 Biology and Life History 441

20.4 Morphological Changes in Stylopised Hosts 444

20.5 Super-stylopisation 444

20.6 Multi-parasitism 444

20.7 Halictophagidae as Biocontrol Agents 445

20.8 Wolbachia Endosymbionts 446

References 449

Index 459